The zoogeography of extant rhabdopleurid hemichordates (Pterobranchia : Graptolithina), with a new species from the Mediterranean Sea
Elena Beli A B G H , Giorgio Aglieri A , Francesca Strano A , Davide Maggioni C D , Max J. Telford E , Stefano Piraino A F G H and Christopher B. Cameron B G H
+ Author Affiliations
- Author Affiliations
A Dipartimento di Scienze e Tecnologie Biologiche ed Ambientali, Università del Salento, Provinciale Lecce – Monteroni, 73100 Lecce, Italy.
B Département de sciences biologiques, Université de Montréal, C.P. 6128, Succursale Centre-ville, Montréal, QC, H3C 3J7, Canada.
C Department of Biotechnology and Biosciences, University of Milano-Bicocca Piazza della Scienza, 2, 20126, Milan, Italy.
D MaRHE Center, University of Milano-Bicocca, Magoodhoo Island, Faafu Atoll, Republic of Maldives.
E Department of Genetics, Evolution and Environment, University College London, Gower Street, London, WC1E 6BT, UK.
F CONISMA, Consorzio Nazionale Interuniversitario per le Scienze del Mare, Piazzale Flaminio 9, 00196 Roma, Italy.
G Senior authors.
H Corresponding authors. Email: elena.beli.sbarra@gmail.com; stefano.piraino@unisalento.it; c.cameron@umontreal.ca
Invertebrate Systematics 32(1) 100-110 https://doi.org/10.1071/IS17021
Submitted: 15 September 2016 Accepted: 31 May 2017 Published: 9 January 2018
Abstract
The early origin and evolutionary radiation of graptolites (Hemichordata : Pterobranchia) is a story told almost entirely in the fossil record, but for four extant species of the genus Rhabdopleura Allman, 1869. Here we report the discovery of a fifth species, Rhabdopleura recondita, sp. nov., at a depth range of 2–70 m from the Adriatic and Ionian Seas, always associated with bryozoans in coralligenous habitats. This is the first pterobranch record in Italian waters, and the second in the Mediterranean Sea. The new species is characterised by: (1) tubaria with smooth creeping tubes adherent to the inside of empty bryozoan zooecia; (2) erect outer tubes with a graptolite, fusellar-like organisation; and (3) zooids that extend from a black stolon, which is free from the creeping tube. Each of the paired feeding arms has two rows of tentacles that do not extend to the arm tip. The distal ends of the arms, the collar and the cephalic shield are replete with black granules. Phylogenetic analyses of individual and concatenated gene sequences of mitochondrial 16S rDNA and nuclear 18S rDNA support the validity of R. recondita as a new species. Finally, we discuss the global biogeographic and habitat distributions of the extant Rhabdopleura representatives.
http://zoobank.org/urn:lsid:zoobank.org:pub:82C6A51E-F8F4-44AF-AD8F-16873BE80D03
Additional keywords: colonial hemichordates, DNA barcoding, integrative taxonomy, morphology, Rhabdopleuridae.
References
Allman, G. J. (1869). On Rhabdopleura, a new form of Polyzoa, from deep-see dredging in Shetland. The Quarterly Journal of Microscopical Science 9, 57–63.Barnes, R. D. (1977). New record of pterobranch hemichordate from the Western hemisphere. Bulletin of Marine Science 27, 340–343.
Burdon-Jones, C. (1954). The habitat and distribution of Rhabdopleura normani Allman. Universitetet I Bergen Årbok Naturvitenskapelig rekke 11, 1–17.
Cameron, C. B. (2005). A phylogeny of the hemichordates based on morphological characters. Canadian Journal of Zoology 83, 196–215.
| A phylogeny of the hemichordates based on morphological characters.Crossref | GoogleScholarGoogle Scholar |
Cannon, J. T., Swalla, B. J., and Halanych, K. M. (2013). Hemichordate molecular phylogeny reveals a novel cold-water clade of harrimaniid acorn worms. The Biological Bulletin 225, 194–204.
| Hemichordate molecular phylogeny reveals a novel cold-water clade of harrimaniid acorn worms.Crossref | GoogleScholarGoogle Scholar |
Cannon, J. T., Kocot, K. M., Waits, D. S., Weese, D. A., Swalla, B. J., Santos, S. R., and Halanych, K. M. (2014). Phylogenomic resolution of the hemichordate and echinoderm clade. Current Biology 24, 2827–2832.
| Phylogenomic resolution of the hemichordate and echinoderm clade.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXhvV2nu73P&md5=2f004b9169813d1a264dfaf6da072905CAS |
Castresana, J. (2000). Selection of conserved blocks from multiple alignments for their use in phylogenetic analysis. Molecular Biology and Evolution 17, 540–552.
| Selection of conserved blocks from multiple alignments for their use in phylogenetic analysis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXisVSgt7g%3D&md5=1b4ae107a4d41c6cf044947b82a73459CAS |
Chapman, A. J., Durman, P. N., and Rickards, R. B. (1995). Rhabdopleuran hemichordates: new fossil forms and review. Proceedings of the Geologists’ Association 106, 293–303.
Darriba, D., Taboada, G. L., Doallo, R., and Posada, D. (2012). jModelTest 2: more models, new heuristics and parallel computing. Nature Methods 9, 772.
| jModelTest 2: more models, new heuristics and parallel computing.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhtFWmsbfP&md5=8455a3ff18c54ee00d48a1421d4dba7aCAS |
De Vito, D., Onofri, I., and Piraino, S. (2010). Una nuova classe di invertebrati per la fauna marina delle acque italiane: prima segnalazione di Rhabdopleura compacta Hincks 1880 (Hemichordata, Pterobranchia) nel Mar Mediterraneo. In ‘71° Congresso Unione Zoologica Italiana, Palermo (Eds N. Parrinello, V. Arizza, M. Cammarata) (20–23 Settembre 2010)’. [In Italian]
Dilly, P. N. (1985). A note on the status of Rhabdopleura from Bermuda. Journal of the Marine Biological Association of the United Kingdom 65, 987–991.
| A note on the status of Rhabdopleura from Bermuda.Crossref | GoogleScholarGoogle Scholar |
Dilly, P. N., and Ryland, J. S. (1985). An intertidal Rhabdopleura (Hemichordata, Pterobranchia) from Fiji. Journal of Zoology 205, 611–623.
| An intertidal Rhabdopleura (Hemichordata, Pterobranchia) from Fiji.Crossref | GoogleScholarGoogle Scholar |
Durman, P. N., and Sennikov, N. V. (1993). A new rhabdopleurid hemichordate from the Middle Cambrian of Siberia. Palaeontology 36, 283–296.
Fatka, O., Kraft, P., and Szabad, M. (2012). A first report of Sphenothallus Hall, 1847 in the Cambrian of Variscan Europe. Comptes Rendus. Palévol 11, 539–547.
| A first report of Sphenothallus Hall, 1847 in the Cambrian of Variscan Europe.Crossref | GoogleScholarGoogle Scholar |
Grieg, J. (1914). Bidrag til kundskaben om Hardangerfjordens fauna. In Burdon-Jones C. (1954). The habitat and distribution of Rhabdopleura normani Allman. Universitetet I Bergen Årbok. Naturvitenskapelig rekke 11, 1–17.
Halanych, K. M. (1995). The phylogenetic position of the pterobranch hemichordates based on 18S rDNA sequence data. Molecular Phylogenetics and Evolution 4, 72–76.
| The phylogenetic position of the pterobranch hemichordates based on 18S rDNA sequence data.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2MXlvFCltr4%3D&md5=2733360b02059bef0b996ac50220e850CAS |
Herdman, W. A. (1892). Notes on the collections made during the cruise of the S.Y. ‘Argo’ up the West Coast of Norway in July, 1891. Proceedings and Transactions of the Liverpool Biological Society 6, 70–95.
Hincks, T. (1880). ‘A History of the British Marine Polyzoa.’ Vol. 1 (John Van Voorst: London.)
Hyman, L. H. (1959). ‘The Invertebrates: Smaller Coelomate Groups – Chaetognatha, Hemichordata, Pogonophora, Phoronida, Ectoprocta, Brachiopoda, Sipunculida – The coelomate Bilateria.’ (McGraw-Hill: New York.)
Johnston, T. H. (1937). A note on the occurrence of Rhabdopleura annulata in South Australian waters. Records of the South Australian Museum 6, 105–107.
Jullien, J. (1890). Description d’un Bryozoaire nouveau du genre Rhabdopleura. Bulletin de la Société Zoologique de France 15, 180–183.
| Description d’un Bryozoaire nouveau du genre Rhabdopleura.Crossref | GoogleScholarGoogle Scholar |
Jullien, J., and Calvet, L. (1903). ‘Bryozoaires provenant des campagnes de l’Hirondelle, 1866–1888. Vol. 23. Résultats des campagnes scientifiques accomplies sur son yacht par Albert Ier, prince souverain de Monaco’ [in French].
Katoh, K., and Standley, D. M. (2013). MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Molecular Biology and Evolution 30, 772–780.
| MAFFT multiple sequence alignment software version 7: improvements in performance and usability.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXksFWisLc%3D&md5=923eb8b83abb772e70745a603d99fa8fCAS |
Kluge, H. (1948). On the occurrence of Rhabdopleura in the Barents Sea. In Stebbing, A. R. D. (1970b). The status and ecology of Rhabdopleura compacta Hincks (Hemichordata), from Plymouth. Journal of the Marine Biological Association of the United Kingdom 50, 209–221.
Köehler, R. (1896). Résultats scientifiques de la campagne du ‘Caudan’ dans le golfe de Gascogne. Annales de l’Université de Lyon 26, 711–740.
Kozłowski, R. (1961). Découverte d’un Rhabdopleuridé (Pterobranchia) ordovicien. Acta Palaeontologica Polonica 6, 3–16.
Lankester, E. R. (1882). Dredging in the Norwegian Fjords. Nature 26, 478–479.
| Dredging in the Norwegian Fjords.Crossref | GoogleScholarGoogle Scholar |
Lankester, E. R. (1884). A contribution to the knowledge of Rhabdopleura. The Quarterly Journal of Microscopical Science 24, 622–647.
Laubier, L. (1964). Découverte de la classe des Ptérobranches en Méditerranée. Comptes Rendus Hebdomadaires des Séances de l’Académie des Sciences 258, 4340–4342.
López-Gappa, J. J. (1987). Presencia del género Rhabdopleura (Hemichordata, Pterobranchia) en la plataforma continental argentina. Physis (Rio de Janeiro, Brazil) 45, 33–36.
Maletz, J. (2014). The classification of the Pterobranchia (Cephalodiscida and Graptolithina). Bulletin of Geosciences 89, 477–540.
| The classification of the Pterobranchia (Cephalodiscida and Graptolithina).Crossref | GoogleScholarGoogle Scholar |
Maletz, J. (2015). Graptolite reconstructions and interpretations. Paläontologische Zeitschrift 89, 271–286.
| Graptolite reconstructions and interpretations.Crossref | GoogleScholarGoogle Scholar |
Maletz, J., and Steiner, M. (2015). Graptolite (Hemichordata, Pterobranchia) preservation and identification in the Cambrian Series 3. Palaeontology 58, 1073–1107.
| Graptolite (Hemichordata, Pterobranchia) preservation and identification in the Cambrian Series 3.Crossref | GoogleScholarGoogle Scholar |
Mierzejewski, P. (1986). Ultrastructure, taxonomy and affinities of some Ordovician and Silurian organic microfossils. Palaeontologia Polonica 47, 129–220.
Mitchell, C. E., Melchin, M. J., Cameron, C. B., and Maletz, J. (2013). Phylogenetic analysis reveals that Rhabdopleura is an extant graptolite. Lethaia 46, 34–56.
| Phylogenetic analysis reveals that Rhabdopleura is an extant graptolite.Crossref | GoogleScholarGoogle Scholar |
Nordgaard, O. (1900). ‘Polyzoa. The Norwegian North-Atlantic Expedition 1876–1878.’ (Grøndhal & Søn: Christiana.)
Norman, A. M. (1869). Shetland final dredging report. Part 2. On the Crustacea, Tunicata, Polyzoa, Echinodermata, Actinozoa, Hydrozoa and Porifera. Reports of the British Association of the Advancement of Science 38, 247–336.
Norman, A. M. (1903). Notes on the natural history of East Finmark. Annals & Magazine of Natural History 12, 87–128.
| Notes on the natural history of East Finmark.Crossref | GoogleScholarGoogle Scholar |
Norman, J. R. (1921). Rhabdopleura. British Antarctic Terra Nova Expedition 1910 (Zoology) 4, 95–102.
Palumbi, S. R. (1996). Nucleic acids II: the polymerase chain reaction. In ‘Molecular Systematics’. (Eds. D. M. Hillis, C. Moritz and B. K. Mable.) pp. 205–247. (Sinauer Associates: Sunderland, MA.)
Rambaut, A., Suchard, M. A., Xie, D., and Drummond, A. J. (2014). ‘Tracer v1.6.’ Available at http://beast.bio.ed.ac.uk/Tracer/
Rickards, R. B., Chapman, A. J., and Temple, J. T. (1984). Rhabdopleura hollandi, a new pterobranch hemichordate from the Silurian of the Llandovery district, Powys, Wales. Proceedings of the Geologists’ Association. Geologists’ Association 95, 23–28.
| Rhabdopleura hollandi, a new pterobranch hemichordate from the Silurian of the Llandovery district, Powys, Wales.Crossref | GoogleScholarGoogle Scholar |
Ronquist, F., Teslenko, M., van der Mark, P., Ayres, D. L., Darling, A., Höhna, S., Larget, B., Liu, L., Suchard, M. A., and Huelsenbeck, J. P. (2012). MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Systematic Biology 61, 539–542.
| MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space.Crossref | GoogleScholarGoogle Scholar |
Sars, G. O. (1874). On Rhabdopleura mirabilis (M. Sars). Quarterly Journal of Microscopical Science. New Series 14, 23–44.
Sato, A., Bishop, J. D. D., and Holland, P. W. H. (2008). Developmental biology of pterobranch hemichordates: history and perspectives. Genesis (New York, N.Y.) 46, 587–591.
| Developmental biology of pterobranch hemichordates: history and perspectives.Crossref | GoogleScholarGoogle Scholar |
Schepotieff, A. (1904). Zur organisation von Rhabdopleura. Bergens Museum Aarbog 2, 1–21.
Schepotieff, A. (1907). Die Pterobranchier. Anatomische und histologische Untersuchungen über Rhabdopleura normani Allman und Cephalodiscus dodecalophus M’int. 1.Teil. Rhabdopleura normani. 1. Abschnitt. Die Anatomie von Rhabdopleura. Zoologische Jahrbücher. Abteilung für Anatomie 23, 463–534.
| Die Pterobranchier. Anatomische und histologische Untersuchungen über Rhabdopleura normani Allman und Cephalodiscus dodecalophus M’int. 1.Teil. Rhabdopleura normani. 1. Abschnitt. Die Anatomie von Rhabdopleura. Zoologische Jahrbücher.Crossref | GoogleScholarGoogle Scholar |
Schepotieff, A. (1909). Die Pterobranchier des Indischen Ozeans. Zoologische Jahrbücher. Abteilung für Systematik 28, 429–448.
Simakov, O., Kawashima, T., Marlétaz, F., Jenkins, J., Koyanagi, R., Mitros, T., Hisata, K., Bredeson, J., Shoguchi, E., Gyoja, F., Yue, J-X., Chen, Y-C., Freeman, R., Sasaki, A., Hikosaka-Katayama, T., Sato, A., Fujie, M., Baughman, K., Levine, J., Gonzalez, P., Cameron, C., Fritzenwanker, J., Pani, A., Goto, H., Kanda, M., Arakaki, N., Yamasaki, S., Qu, J., Cree, A., Ding, Y., Dinh, H., Dugan, S., Holder, M., Jhangiani, S., Kovar, C., Lee, S., Lewis, L., Morton, D., Nazareth, L., Okwuonu, G., Santibanez, J., Chen, R., Richards, S., Muzny, D., Gillis, A., Peshkin, L., Wu, M., Humphreys, T., Su, Y-H., Putnam, N., Schmutz, J., Fujiyama, A., Yu, Jr-K., Tagawa, K., Worley, K., Gibbs, R., Kirschner, M., Lowe, C., Satoh, N., Rokhsar, D., and Gerhart, J. (2015). Hemichordate genomes and deuterostome origins. Nature 527, 459–465.
| Hemichordate genomes and deuterostome origins.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXhvVKrtbnP&md5=4a949367a65ff88dec4da3bd2b5b68a5CAS |
Stebbing, A. R. D. (1968). Discovery of Rhabdopleura (Hemichordata) at Plymouth. Nature 217, 1284.
| Discovery of Rhabdopleura (Hemichordata) at Plymouth.Crossref | GoogleScholarGoogle Scholar |
Stebbing, A. R. D. (1970a). Aspects of the reproduction and life cycle of Rhabdopleura compacta (Hemichordata). Marine Biology 5, 205–212.
| Aspects of the reproduction and life cycle of Rhabdopleura compacta (Hemichordata).Crossref | GoogleScholarGoogle Scholar |
Stebbing, A. R. D. (1970b). The status and ecology of Rhabdopleura compacta (Hemichordata), from Plymouth. Journal of the Marine Biological Association of the United Kingdom 50, 209–221.
| The status and ecology of Rhabdopleura compacta (Hemichordata), from Plymouth.Crossref | GoogleScholarGoogle Scholar |
Stebbing, A. R. D., and Dilly, P. N. (1972). Some observations on living Rhabdopleura compacta (Hemichordata). Journal of the Marine Biological Association of the United Kingdom 52, 443–448.
| Some observations on living Rhabdopleura compacta (Hemichordata).Crossref | GoogleScholarGoogle Scholar |
Sukumaran, J., and Holder, M. T. (2010). DendroPy: a Python library for phylogenetic computing. Bioinformatics 26, 1569–1571.
| DendroPy: a Python library for phylogenetic computing.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXnsVOltb0%3D&md5=a27eb353ecdc058e87bd195941b4e5e2CAS |
Talavera, G., and Castresana, J. (2007). Improvement of phylogenies after removing divergent and ambiguously aligned blocks from protein sequence alignments. Systematic Biology 56, 564–577.
| Improvement of phylogenies after removing divergent and ambiguously aligned blocks from protein sequence alignments.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXhtFKrs7%2FP&md5=0dced01d514658b36c15b77c9c96df0fCAS |
Tamura, K., Stecher, G., Peterson, D., Filipski, A., and Kumar, S. (2013). MEGA6: molecular evolutionary genetics analysis version 6.0. Molecular Biology and Evolution 30, 2725–2729.
| MEGA6: molecular evolutionary genetics analysis version 6.0.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhvVKhurzP&md5=213a455e206e1c198319858e32755a17CAS |
Urbanek, A., and Dilly, P. N. (2000). The stolon system in Rhabdopleura compacta (Hemichordata) and its phylogenetic implications. Acta Palaeontologica Polonica 45, 201–226.
van der Horst, C. J. (1939). Hemichordata. In ‘Klassen und Ordnungen des Tier-Reichs wissenschaftlich dargestellt in Wort und Bild’. (Eds H.G. Bronns.) Band 4, Abt. 4, Buch 2, Tiel 2. p. 737 [in German]. (Akademische Verlagsgesellschaft, Leipzig.)
Van Soest, R. W. M., Boury-Esnault, N., Vacelet, J., Dohrmann, M., Erpenbeck, D., De Voogd, N. J., Santodomingo, N., Vanhoorne, B., Kelly, M., and Hooper, J. N. A. (2012). Global diversity of sponges (Porifera). PLoS One 7, e35105.
| Global diversity of sponges (Porifera).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XntVemtrs%3D&md5=e5209766e71a84ecdd66c0f51d2fd992CAS |
Zietara, M. S., Arndt, A., Geets, A., Hellemans, B., and Volckaert, F. A. (2000). The nuclear rDNA region of Gyrodactylus arcuatus and G. branchicus (Monogenea: Gyrodactylidae). The Journal of Parasitology 86, 1368–1373.
| The nuclear rDNA region of Gyrodactylus arcuatus and G. branchicus (Monogenea: Gyrodactylidae).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXltFKksQ%3D%3D&md5=9b263457a62c895658b28efb6f376759CAS |
Zwickl, D. J. (2006). Genetic algorithm approaches for the phylogenetic analysis of large biological sequence datasets under the maximum likelihood criterion. Ph.D. Thesis, University of Texas at Austin, USA.
